Why a new volume on non-pollen palynomorphs?

Why a new volume on non-pollen palynomorphs (NPPs)? Quite simply because there isn't one. Most especially not one that bridges the gaps between the use of NPPs in Quaternary and pre-Quaternary studies.

NPPs are an increasingly important part of archaeological, palaeoecological, palaeoclimatic, and biostratigraphic studies throughout the geological and archaeological record. While recognized in the fossil record for nearly two centuries, it is only in the past 75 years that marine dinoflagellate cysts have become robust biostratigraphic and palaeoecological proxies throughout the rock record, as have other marine NPPs such as Acritarchs, Prasinophytes, Chitinozoa, and Scolecodonts. Application of terrestrial NPP groups, especially in deep time, has been sporadic at best, although archaeologists, and Quaternary geologists and palaeoecologists have made significant strides in the past 30 years, thanks in a very large part to the work of Bas van Geel (1978, 1979, 1998, 2001, Fig. 1) and his students and colleagues (van Geel and van der Hammen 1978; van Geel et al. 1994, 1996, 2011; van Geel and Grenfell 1996; van Hoeve and Hendrikse 1998; van Geel and Aptroot 2006, among many others). This early work catalysed Russian Quaternary palaeoecologists (Kats et al. 1977). A similar effort, focused on fungi only, was seen among Canadian, Indian and American deep-time geologists (Fig. 2). However, as the focus of groups led by Jansonius (1962, 1976), Elsik (1968, 1970, 1976a, b, 1992, 1996), Elsik and Jansonius (1974), Kalgutkar (1985), Kalgutkar and Sweet (1988), Kalgutkar and McIntyre (1991), Kalgutkar and Jansonius (2000) and Saxena (1991, 2006, 2019) was largely biostratigraphic, and the majority of these scientists were not at universities, their work was not as widely adopted. Of note, both recent schools of NPP study appear to have been catalysed, at least in part, by the work of Graham (1962), who in turn had studied works stretching as far back as 1850, and Frey (1964). Recent advances in palynological processing (see Pound et al. 2021), changes in approach to nomenclature (see O'Keefe et al. 2021), especially for fossil fungi, and collaborations with mycologists (see Nuñez Otaño et al. 2021) and protistologists (see Andrews et al. 2021) have allowed the recognition of many NPPs deeper in the rock record. Indeed, some of the earliest recorded forms of life are NPPs – acid-resistant carbonaceous spheres in Archean rocks (Javeaux et al. 2010; Agić and Cohen 2021 ).

The name ‘non-pollen palynomorph’, in many ways, is based on the assumption that pollen are most important for palynological, especially palaeoecological, studies. This is a uniquely Quaternary viewpoint. Indeed, while pollen was described by Malphigi and Grew in 1675–82 (Malpighi 1675, 1679; Grew 1682), what we now call NPPs began to be described very soon thereafter (Fig. 3), beginning with pteridophyte and fungal spores by Tournefort in the 1690s and Geoffroy in the early 1700s (Geoffroy 1714; Stroup 1990; Bernasconi and Taiz 2006) and dinoflagellates in the mid-1700s (Baker 1753; Rochon et al. 2013). The first fossil pollen were described from thin-sections of coal in 1833 by Witham (1833), although they were initially described as resin vessels. The first undisputed fossil pollen were described and illustrated by line drawings in 1836 by Göppert as part of a study of fossil plants. Dinoflagellate cysts and acritarchs were described near-simultaneously by Ehrenberg (Fig. 4a; Ehrenberg 1837; Sarjeant 2002; Traverse 2007); these studies culminated with the publication of Mikrogeologie in 1854 (Ehrenberg 1854). Fossil microfungi were first described in 1848 (Fig. 4b; Berkeley 1848; Taylor et al. 2015), and their study progressed to parallel that of fossil pollen through the early 1900s. The late 1840s and early 1850s were an era of discovery; in addition to those named above, many other NPPs were identified for the first time, largely through the efforts of microscopy clubs, such as that in Clapham, UK (Sarjeant 1991): foraminiferal linings and Botryococcus algae were both described in 1849; prasinophytes were described in 1852; and scolecodonts in 1854 (Sarjeant 2002). In the early years, emphasis was on documenting all the microscopic taxa recovered in the course of a study, whether it be from a modern lake or bog or from Pleistocene peats or from Carboniferous coals. This trend continued through the earliest part of the 1900s as additional NPPs, including testate amoebae, spermatophores of copepods, and Rhabdocoelan oocytes (Rudolph 1917), were described in Quaternary bogs and peats. While changes were in the air, discovery continued, with heliozoans, Macrobiotus sp. eggs, and chytrids on pollen walls being described in the late 1920s (Hesmer 1929) and chitinozoans in 1931 (Fig. 4c; Eisenack 1931; Sarjeant 2002).

Quaternary palaeoecology began to blossom in the 1890s and early 1900s in Sweden, Denmark, Finland and Germany with the recognition that different layers of sediment from bogs preserved different quantities and assemblages of palynomorphs (Weber 1893, 1896; Lagerheim 1895; Sarauw 1897; Lindberg 1900; Witte 1905; Holst 1908). With the publication of Von Post's (1916, 1918) papers, Quaternary palaeoecology, firmly tied to the pollen record, was born (Edwards 2018), and solidified through the work of his colleagues and students, most notably Erdtman (1925), Sarjeant (2002) and Traverse (2007). Despite this emphasis on pollen, studies of NPPs occurring in palynology slides continued, albeit sporadically, until renewed interest in them began in the 1960s.

Palaeopalynology had begun to diverge from actuopalynology at about the same time as Quaternary palaeoecology developed, beginning with adoption of the artificial nomenclatural scheme originally proposed by Reinsch, Bennie and Kidston in the 1880s, first used by H. Potonié in the 1890s, and subsequently by palaeobotanists, especially Bartlett, in the 1920s (Bennie and Kidston 1886; Bartlett 1929a, b; Sarjeant 2002; see O'Keefe et al. 2021), and continuing with the recognition that palynomorphs could be useful in correlating coal seams beginning in 1918 (Thiessen 1918, 1920; Thiessen and Staud 1923). This realization, which came into its own in England and Germany from cross-fertilization due to visits in the mid-1920s from both Thiessen, to Sheffield and many other places (Lyons and Teichmüller 1995), and Erdtman, to various universities, including Leeds, where he worked closely with the botany and palynology group led by Burrell (Cross and Kosanke 1995; Marshall 2005). This knowledge was carried to the USA by both Erdtman himself and a young student named L.R. Wilson, who happened to be studying at the University of Leeds with Burrell immediately following Erdtman's visit (Cross and Kosanke 1995). While trained as an actuopalynologist, L.R. Wilson turned his attention to palaeopalynology beginning with a 1937 study of palynomorphs from a coal seam in Iowa (Wilson and Brokaw 1937), and collaborated with J.M. Schopf, who had himself begun to study palynomorphs in 1936, eventually producing a seminal work on Carboniferous spores in the Illinois Basin (Schopf et al. 1944). By 1944, however, palynostratigraphy had become the major emphasis in deep-time palynology (Wilson 1944). Interestingly, the development of palaeopalynology in Britain also began at Leeds around the same time, when A. Raistrick was a student and young researcher there. Raistrick began publishing palynological studies in the 1930s and, like Wilson, began with actuopalynological studies of peat before progressing to studies of Carboniferous spores (Raistrick and Woodhead 1930; Raistrick 1933a, b, 1934a, b, 1935, 1936, 1937, 1938, 1939; Marshall 2005). Raistrick, along with his collaborator Kathleen Blackburn, continued work on palynology ranging from Quaternary to Carboniferous studies after his move to Newcastle; a key addition in terms of NPP research was their confirmation that the Carboniferous algae noted by Thiessen many years earlier were indeed Botryococcus, and indistinguishable from their modern counterparts (Marshall 2005). Again, during the same period in the mid-1920s, I. Cookson was in residence in Britain, first at Imperial College London, then at the University of Manchester (Dettmann 1993; Riding and Dettmann 2013); it is likely that she, too, was catalysed by lectures from Erdtman and Thiessen, although her interest in fossil plants and fungi was already developing. Cookson was trained as a modern botanist and mycologist in Australia, but turned her attention to palaeobotany and palaeomycology while in the UK; this collaboration produced many notable works, most importantly her seminal paper on Cenozoic fungi (1947). Near-simultaneously, in Germany, R. Potonié, beginning with his 1931 papers (Potonié 1931a, b, c), demonstrated the utility of palynostratigraphy and correlation in Paleogene coal-bearing sediments; these studies used the system of form-nomenclature propounded by Bartlett, which rapidly became entrenched in palaeopalynology – thus, not only were actuopalynologists and deep-time palynologists going in different directions, from the 1930s onward, they were speaking separate languages (see O'Keefe et al. 2021), and much of the early cross-fertilization of ideas began to wane.

Elsewhere in the world, studies of pre-Quaternary NPPs, primarily spores, acritarchs, chitinozoans, dinoflagellate cysts and prasinophytes, began in earnest in the lead-up to World War II (Sarjeant 2002). In Russia, much of this early work was led by Naumova (1939) and Liuber (1938), with an emphasis on late Paleozoic spores and pre-pollen. In India, pioneering work by Virkki (1937), a student of Birbal Sahni, on Permian floras set the stage for an explosion of palaeopalynological studies in that country. Dinoflagellate cyst studies experienced a renaissance in the 1930s, beginning with the work of Wetzel (1932, 1933a, b), Deflandre (1935, 1936, 1937), Lejeune (1936) and Eisenack (1931, 1935, 1936a, b), and Lewis (1940), and early explorations of their utility as biostratigraphic indicators by Shell Oil (Sarjeant 2002), although WWII put a hiatus on much progress. It was not until the nestor of dinoflagellate studies, W. Evitt, turned his attention to their biology and geology in the late 1950s that their study blossomed into the robust community it is today (Riding and Lucas-Clark 2016). His work catalysed fellow dinoflagellate workers Downie, Gocht, Hughes, Rossignol, Sarjeant, Vozzhennikova, Wetzel, among others (Sarjeant 2002), and led to the establishment of two major centres of fossil dinoflagellate research: (1) Stanford University in the USA and (2) the University of Sheffield in the UK. Downie's research group at Sheffield was instrumental in advancing acritarch research following WWII, as were Naumova in Moscow and Timofeyev in Leningrad, and many others in mainland Europe. Prasinophyte research did not make many advances until the post-war era, when some 14 genera were named in the period from 1952–67 (Guy-Ohlson 1996; Sarjeant 2002). It was also in this period that the origin of Scolecodonts was realized after Lange (1947, 1949) and Kozlowski (1956) presented articulated jaws from the Devonian of Brazil and Ordovician of Poland, respectively, and further study in Poland led to Kielan-Jaworowska's (1966) seminal work on the preliminary phylogeny of this group. However, much of this phylogeny is now obsolete and the phylogeny and classification of scolecodonts is part and parcel of the study of fossil annelids (Parry et al. 2019), as is the study of clitellate cocoons, although these cocoons are of limited taxonomic value in and of themselves. Studies of Chitinozoa, too, blossomed in the post-war period, and continue to be robust biostratigraphic markers throughout their range, although their affinity remains unknown, although the consensus is that they are the remains of an extinct organism (Liang et al. 2019). By the late 1960s and early 1970s, study of NPPs, in both geological and Quaternary contexts was coming into its own and, through the early 2000s, has become increasingly important in palaeoecological studies.

For much of the fossil record, it is NPPs that are dominant, and their diversification parallels the development of multicellular life and land plants (Table 1, Fig. 5). Beginning with the simple spherical carbonaceous forms noted by Javeaux et al. (2010), both marine and terrestrial NPPs, including acritarchs, monolete and trilete plant spores, have been keys to understanding the oxygenation of Earth's atmosphere (Agić and Cohen 2021), rise of multicellular life in the oceans (Agić and Cohen 2021 ), and the invasion of land (Wellman and Ball 2021 ). Indeed, Precambrian through Paleozoic biostratigraphic studies rely on NPPs, including acritarchs, chitinozoans, and precursors to dinoflagellates (Huntley et al. 2006; Knoll et al. 2007; Molyneux et al. 2013; Servais et al. 2013), as do Mesozoic and Cenozoic studies of marine sediments (Hubbard et al. 1994; Penaud et al. 2018). Thus, the evolutionary history of NPP groups is the evolutionary history of the earliest life, and a vibrant record of its diversification and preservation in the rock record.

To date, no compendium addressing NPPs and their utilities from modern to ancient applications exists. This book endeavours to fill the gap by providing 12 review papers on the use and identification of NPPs. It is arranged in three sections. The first contains three background chapters: an overview of what organismal remains are considered NPPs (Shumilovskikh et al. 2021 ), how processing impacts the NPP spectrum obtained by the researcher (Pound et al. 2021 ) and a historical overview of nomenclature and recommendations for naming NPPs moving forward (O'Keefe et al. 2021 ). These chapters provide necessary background for current and student NPP researchers and context for interpreting what is known about NPP occurrence and utility as proxies. The second section contains an overview of the major groups of NPPs: fungi (Nuñez Otaño et al. 2021 ); freshwater remains including dinoflagellates, tintinnids, euglenids, arcellinids, rotifers thecae and eggs, flatworm egg cases, nematode eggs, and the remains of cladocerans and diptera (McCarthy et al. 2021 ); testate amoebae (Andrews et al. 2021 ); marine remains including dinoflagellates, acritarchs, tintinnids, ostracod and foraminiferal linings, copepods, and worm remains (Mudie et al. 2021 ). These chapters provide in-depth overviews of the major NPP groups in the context of their occurrence (terrestrial or marine). They are invaluable resources for understanding the intricacies of each taxon as a proxy and interpreting their distribution in rocks and sediments. The third section provides reviews of state of the art of application of NPPs to a variety of problems: interpreting human impact on the environment (Gauthier and Jouffroy-Bapicot 2021 ); using coprophilous fungal spores to study megaherbivores (van Asperen et al. 2021 ); examining NPP distribution in marine settings across a major hyperthermal event (Denison 2021 ); tracing the origin and distribution of early land plants (Wellman and Ball 2021 ); and tracing the origin of early life and eukaryotes (Agić and Cohen 2021 ).

Development of this book was not without its unforeseen challenges. The COVID-19 pandemic struck just as papers were being finalized for submission, significantly slowing the process as several co-authors and their families battled for their health and sanity during repeated global, regional and local shut-downs as well as a transition to primarily online course delivery and/or working remotely. We thank our many contributors, reviewers, production staff and families for their patience and support during the lengthy process.

JMKO: conceptualization (equal), writing – original draft (lead), writing – review & editing (lead); FM: conceptualization (equal), writing – original draft (supporting), writing – review & editing (supporting); PO: conceptualization (equal), writing – review & editing (supporting); MJP: conceptualization (equal), writing – review & editing (equal); LS: conceptualization (equal), writing – review & editing (supporting).

This research received no specific grant from any funding agency in the public, commercial, or not-for-profit sectors.

Data sharing is not applicable to this article as no datasets were generated or analysed during the current study.